Reproductive ecology of the black rat (Rattus rattus) in Madagascar: the influence of density-dependent and -independent effects
Kathryn SCOBIE, Soanandrasana RAHELINIRINA, Voahangy SOARIMALALA, Fehivola Mandanirina ANDRIAMIARIMANANA, Corinne RAHAINGOSOAMAMITIANA, Toky RANDRIAMORIA, Soloandry RAHAJANDRAIBE, Xavier LAMBIN, Minoarisoa RAJERISON, Sandra TELFER
Reproductive ecology of the black rat (Rattus rattus) in Madagascar: the influence of density-dependent and -independent effects
The black rat (Rattus rattus) poses a severe threat to food security and public health in Madagascar, where it is a major cause of pre- and post-harvest crop losses and an important reservoir for many zoonotic diseases, including plague. Elsewhere, ecologically based rodent management (EBRM) strategies have been developed using ecological information to inform decisions on where and when to target control. EBRM could deliver improved health and well-being outcomes in Madagascar if adapted to the local ecological context. Using data collected from removal studies, we explored spatio-temporal patterns in the breeding activity of the black rat (R. rattus) in domestic and agricultural habitats across Madagascar and investigated to what extent these trends are influenced by rainfall and rat density. We identified clear spatio-temporal variation in the seasonality of R. rattus reproduction. Reproduction was highly seasonal both inside and outside of houses, but seasonal trends varied between these two habitats. Seasonal trends were explained, in part, by variation in rainfall; however, the effect of rainfall on reproductive rates did itself vary by season and habitat type. A decline in breeding intensity with increasing rat density was recorded outside of houses. This has important implications for control, as populations may compensate for removal through increased reproduction. We recommend that sustained control initiated before the main breeding season, combined with improved hygiene and adequate rodent-proofing in homes and grain stores, could curtail population growth and reduce pre- and post-harvest losses provided that these measures overcome the compensatory response of rodent populations.
Madagascar / Rattus rattus / reproductive ecology / rodent control
[1] |
Adler GH (1998). Impacts of resource abundance on populations of a tropical forest rodent. Ecology 79, 242–54.
|
[2] |
Andreo V, Lima M, Provensal C, Priotto J, Polop J (2009a). Population dynamics of two rodent species in agro-ecosystems of central Argentina: Intra-specific competition, land-use, and climate effects. Population Ecology 51, 297–306.
|
[3] |
Andreo V, Provensal C, Scavuzzo M, Lamfri M, Polop J (2009b). Environmental factors and population fluctuations of Akodon azarae (Muridae: Sigmodontinae) in central Argentina. Austral Ecology 34, 132–42.
|
[4] |
Andrianaivoarimanana V, Kreppel K, Elissa N et al. (2013). Understanding the persistence of plague foci in Madagascar. PLoS Neglected Tropical Diseases 7, e2382.
|
[5] |
Aplin K, Lalsiamliana J (2010). Chronical and impacts of the 2005–09 mautam in Mizoram. In: Singleton GR, Belmain SR, Brown PR, Hardy B, eds. Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Baños, the Philippines, pp. 13–47.
|
[6] |
Arnold TW (2010). Uninformative parameters and model selection using Akaike's information criterion. Journal of Wildlife Management 74, 1175–8.
|
[7] |
Barton K (2020). MuMIn: Multi-model inference. R package version 1.43.17. Available from URL:
|
[8] |
Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF (2018). Present and future Köppen-Geiger climate classification maps at 1-km resolution. Scientific Data 5, 180214.
|
[9] |
Belmain SR (2010). Developing pesticide-free rodent control for southern Africa. Pesticides News 87, 9–11.
|
[10] |
Belmain SR, Chakma N, Sarker NJ et al. (2010). The Chittagong story: Studies on the ecology of rat floods and bamboo masting. In: Singleton GR, Belmain SR, Brown PR, Hardy B, eds. Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Baños, the Philippines, pp. 49–63.
|
[11] |
Belmain SR, Htwe NM, Kamal NQ, Singleton GR (2015). Estimating rodent losses to stored rice as a means to assess efficacy of rodent management. Wildlife Research 42, 132–42.
|
[12] |
Belmain SR, Meyer AN, Timbrine R, Penicela L (2003). Managing rodent pests in households and food stores through intensive trapping. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM, eds. Rats, Mice and People: Rodent Biology and Management. Australian Centre for International Agricultural Research, Canberra, pp. 440–5.
|
[13] |
Belmain SR, Ndiaye CF, Diallo B et al. (2018). A New Rat Control Strategy for Madagascar to Prevent Plague Outbreaks. Organisation Mondiale de la Santé, Antananarivo, 23 p.
|
[14] |
Bielby J, Vial F, Woodroffe R et al. (2016). Localised badger culling increases risk of herd breakdown on nearby, not focal, land. PLoS ONE 11, e0164618.
|
[15] |
Brooks ME, Kristensen K, van Benthem KJ et al. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9, 378–400.
|
[16] |
Brouat C, Rahelinirina S, Loiseau A et al. (2013). Plague circulation and population genetics of the reservoir Rattus rattus: The influence of topographic relief on the distribution of the disease within the Madagascan focus. PLoS Neglected Tropical Diseases 7, e2266.
|
[17] |
Brown PR, Tuan NP (2005). Compensation of rodent pests after removal: Control of two rat species in an irrigated farming system in the Red River Delta, Vietnam. Acta Oecologica 28, 267–79.
|
[18] |
Brown PR, Tuan NP, Singleton GR et al. (2005). Population dynamics of Rattus argentiventer, Rattus losea, and Rattus rattus inhabiting a mixed-farming system in the Red River Delta, Vietnam. Population Ecology 47, 247–56.
|
[19] |
Brown PR, Tuan NP, Singleton GR et al. (2006). Ecologically based management of rodents in the real world: Applied to a mixed agroecosystem in Vietnam. Ecological Applications 16, 2000–10.
|
[20] |
Burnham KP, Anderson DR, eds (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer-Verlag, Heidelberg.
|
[21] |
Capizzi D, Bertolino S, Mortelliti A (2014). Rating the rat: Global patterns and research priorities in impacts and management of rodent pests. Mammal Review 44, 148–62.
|
[22] |
Chanteau S, Rahalison L, Duplantier JM et al. (1998). Actualités sur la peste à Madagascar. Médecine Tropicale 58, 25–31.
|
[23] |
Clapperton BK (2006). A review of the current knowledge of rodent behaviour in relation to control devices. Science for Conservation 263, 1–55.
|
[24] |
Clark DA (1980). Foraging patterns of black rats across a desert-montane forest gradient in the Galapagos Islands. Biotropica 13, 182–94.
|
[25] |
Constant NL, Swanepoel LH, Williams ST et al. (2020). Comparative assessment on rodent impacts and cultural perceptions of ecologically based rodent management in 3 Afro-Malagasy farming regions. Integrative Zoology 15, 578–94.
|
[26] |
Courchamp F, Clutton-Brock T, Grenfell B (1999). Inverse density dependence and the Allee effect. Trends in Ecology & Evolution 14, 405–10.
|
[27] |
Donnelly CA, Woodroffe R, Cox DR et al. (2006). Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439, 843–6.
|
[28] |
Douangboupha B (2010). Rodent outbreaks in the uplands of Lao PDR. In: Singleton GR, Belmain SR, Brown PR, Hardy B, eds. Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Baños, the Philippines, pp. 99–109.
|
[29] |
Duplantier J-M, Duchemin JB, Chanteau S, Carniel E (2005). From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague re-emergence. Veterinary Research 36, 437–53.
|
[30] |
Duplantier J-M, Rakotondravony D (1999). The rodent problem in Madagascar: Agricultural pest and threat to human health. In: Singleton GR, Hinds LA, Leirs H, Zhang Z, eds. Ecologically-Based Management of Rodent Pests. ACIAR Monograph No. 59. Australian Centre for International Agricultural Research, Canberra, pp. 441–57.
|
[31] |
Duron Q, Cornulier T, Vidal E, Bourguet E, Ruffino L (2020). Combining live and lethal trapping to inform the management of alien invasive rodent populations in a tropical montane forest. NeoBiota 63, 101–25.
|
[32] |
Funk C, Peterson P, Landsfeld M et al. (2015). The climate hazards infrared precipitation with stations—A new environmental record for monitoring extremes. Scientific Data 2, 150066.
|
[33] |
Gomez MD, Priotto J, Provensal MC, Steinmann A, Castillo E, Polop JJ (2008). A population study of house mice (Mus musculus) inhabiting different habitats in an Argentine urban area. International Biodeterioration & Biodegradation 62, 270–3.
|
[34] |
Hartig F (2021). DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.4.4. Available from URL:
|
[35] |
Harvey CA, Rakotobe ZL, Rao NS et al. (2014). Extreme vulnerability of smallholder farmers to agricultural risks and climate change in Madagascar. Philosophical Transactions of the Royal Society of London B: Biological Sciences 369, 20130089.
|
[36] |
Hieronimo P, Kihupi NI, Kimaro DN et al. (2014). Contribution of land use to rodent flea load distribution in the plague endemic area of Lushoto District, Tanzania. Tanzania Journal of Health Research 16, 240–9.
|
[37] |
Htwe N, Singleton G, Thwe A, Lwin Y (2010). Rodent population outbreaks associated with bamboo flowering in Chin State, Myanmar. In: Singleton GR, Belmain SR, Brown PR, Hardy B, eds. Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Baños, the Philippines, pp. 79–97.
|
[38] |
Htwe NM, Sarathchandra SR, Sluydts V, Nugaliyadde L, Singleton GR, Jacob J (2021). Small mammal communities, associated damage to rice and damage prevention in smallholder rice storage facilities in Sri Lanka. Crop Protection 145, 105638.
|
[39] |
Htwe NM, Singleton GR (2014). Is quantity or quality of food influencing the reproduction of rice-field rats in the Philippines? Wildlife Research 41, 56–63.
|
[40] |
Htwe NM, Singleton GR, Hinds LA, Propper CR, Sluydts V (2012). Breeding ecology of rice field rats, Rattus argentiventer and R. tanezumi in low-land irrigated rice systems in the Philippines. Agriculture Ecosystems and Environment 161, 39–45.
|
[41] |
Huan NH, Nga VTQ, Brown PR, My Phung NT, Singleton GR (2010). Rodent impacts in lowland irrigated intensive rice systems in Vietnam. In: Singleton GR, Belmain SR, Brown PR, Hardy B, eds. Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Baños, the Philippines, pp. 139–52.
|
[42] |
Jaksic FM, Lima M (2003). Myths and facts on ratadas: Bamboo blooms, rainfall peaks and rodent outbreaks in South America. Austral Ecology 28, 237–51.
|
[43] |
Khamphoukeo K, Brown PR, Douangboupha B, Aplin KP, Singleton GR (2006). Population dynamics of rodent pests in upland farming systems of Lao PDR. Lao Journal of Agriculture and Forestry 12, 109–21.
|
[44] |
Krebs CJ, Redfield JA, Taitt MJ (1978). A pulsed-removal experiment on the vole Microtus townsendii. Canadian Journal of Zoology 56, 2253–62.
|
[45] |
Lee MJ, Byers KA, Donovan CM et al. (2018). Effects of culling on Leptospira interrogans carriage by rats. Emerging Infectious Diseases 24, 356–60.
|
[46] |
Leirs H, Stenseth NC, Nichols JD, Hines JE, Verhagen R, Verheyen W (1997). Stochastic seasonality and nonlinear density-dependent factors regulate population size in an African rodent. Nature 389, 176–80.
|
[47] |
Leroux SJ (2019). On the prevalence of uninformative parameters in statistical models applying model selection in applied ecology. PLoS ONE 14, e0206711.
|
[48] |
Leung LK-P, Singleton GR, Sudarmaji R (1999). Ecologically-based population management of the rice-field rat in Indonesia. In: Singleton GR, Belmain SR, Brown PR, Hardy B, eds. Rodent Outbreaks: Ecology and Impacts. International Rice Research Institute, Los Baños, the Philippines, pp. 305–18.
|
[49] |
Lewellen RH, Vessey SH (1998). The effect of density dependence and weather on population size of a polyvoltine species. Ecological Monographs 6, 571–94.
|
[50] |
Meerburg BG, Singleton GR, Kijlstra A (2009). Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35, 221–70.
|
[51] |
Melero Y, Robinson E, Lambin X (2015). Density-and age-dependent reproduction partially compensates culling efforts of invasive non-native American mink. Biological Invasions 17, 2645–57.
|
[52] |
Miarinjara A, Boyer S (2016). Current perspectives on plague vector control in Madagascar: Susceptibility status of Xenopsylla cheopis to 12 insecticides. PLoS Neglected Tropical Diseases 10, e0004414.
|
[53] |
Miller CJ, Miller TK (1995). Population dynamics and diet of rodents on Rangitoto Island, New Zealand, including the effect of a 1080 poison operation. New Zealand Journal of Ecology 19, 19–27.
|
[54] |
Morris DW (2002). Measuring the Allee effect: Positive density dependence in small mammals. Ecology 83, 14–20.
|
[55] |
Ostfeld RS, Canham CD (1995). Density-dependent processes in meadow voles: An experimental approach. Ecology 76, 521–32.
|
[56] |
Palis FG, Singleton GR, Brown PR, Huan NH, Umali C, Nga NTD (2011). Can humans outsmart rodents? Learning to work collectively and strategically. Wildlife Research 38, 568–78.
|
[57] |
Panti-May JA, Hernández-Betancourt S, Ruíz-Piña H, Medina-Peralta S (2012). Abundance and population parameters of commensal rodents present in rural households in Yucatan, Mexico. International Biodeterioration and Biodegradation 66, 77–81.
|
[58] |
Peel MC, Finlayson BL, McMahon TA (2007). Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11, 1633–44.
|
[59] |
Pocock MJO, Searle JB, White PCL (2004), Adaptations of animals to commensal habitats: Population dynamics of house mice Mus musculus domesticus on farms. Journal of Animal Ecology 73, 878–88.
|
[60] |
Previtali MA, Meserve PL, Kelt DA, Gutierrez ML Jr (2009). Population dynamics of two sympatric rodent species in a highly variable environment: The influence of rainfall, resource availability, and predation. Ecology 90, 1996–2006.
|
[61] |
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from
|
[62] |
Rahelinirina S, Duplantier JM, Ratovonjato J, Ramilijaona O, Ratsimba M, Rahalison L (2010). Study on the movement of Rattus rattus and evaluation of the plague dispersion in Madagascar. Vector-Borne and Zoonotic Diseases 10, 77–84.
|
[63] |
Rahelinirina S, Rajerison M, Telfer S, Savin C, Carniel E, Duplantier J (2017). The Asian house shrew Suncus murinus as a reservoir and source of human outbreaks of plague in Madagascar. PLoS Neglected Tropical Disease 11, e0006072.
|
[64] |
Rahelinirina S, Scobie K, Ramasindrazana B et al. (2021). Rodent control to fight plague: Field assessment of methods based on rat density reduction. Integrative Zoology 16, 868–85.
|
[65] |
Rajonhson DM, Miarinjara A, Rahelinirina S, Rajerison M, Boyer S (2017). Effectiveness of fipronil as a systemic control agent against Xenopsylla cheopis (Siphonaptera: Pulicidae) in Madagascar. Journal of Medical Entomology 54, 411–7.
|
[66] |
Rasolozaka IN (1999). Biologie et migration des rats dans les polycultures de la côte Est. In: Rongeurs et Lutte Antimurine à Madagascar. Actes du Symposium National sur les Rongeurs et la lute Anti Murine, DPV et GTZ, Tome II; Antananarivo, Madagascar, pp. 59–67.
|
[67] |
Ratsimanosika L (1999). Biologie et migration des rats dans la rizi-culture de Manaratsandry/Marovoay. In: Actes du Symposium National sur les Rongeurs et la lute Anti Murine, DPV et GTZ, Tome II; Antananarivo, Madagascar, pp. 69–90.
|
[68] |
Richards SA, Whittingham MJ, Stephens PA (2011). Model selection and model averaging in behavioural ecology: The utility of the IT-AIC framework. Behavioral Ecology and Sociobiology 65, 77–89.
|
[69] |
Rigden AJ, Golden C, Huybers P (2022). Retrospective predictions of rice and other crop production in Madagascar using soil moisture and an NDVI-based calendar from 2010–2017. Remote Sensing 14, 1223.
|
[70] |
Sikes RB, Gannon WL, the Animal Care and Use Committee of the American Society of Mammalogists (2016). Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97, 663–88.
|
[71] |
Singleton GR, Brown PR, Jacob J, Aplin KP, Sudarmaji
|
[72] |
Singleton GR, Jacob J, Krebs CJ (2005). Integrated management to reduce rodent damage to lowland rice crops in Indonesia. Agriculture, Ecosystems and Environment 107, 75–82.
|
[73] |
Singleton GR, Leirs H, Hinds LA, Zhang ZB (1999). Ecologically-based management of rodent pests—Re-evaluating our approach to an old problem. In: Singleton GR, Hinds LA, Leirs H, Zhang Z, eds. Ecologically-Based Management of Rodent Pests. ACIAR Monograph No. 59. Australian Centre for International Agricultural Research, Canberra, pp. 1–50.
|
[74] |
Sluydts V, Crespin L, Davis S, Lima M, Leirs H (2007). Survival and maturation rates of the African rodent, Mastomys natalensis: Density-dependence and rainfall. Integrative Zoology 2, 220–32.
|
[75] |
Smith GC, Delahay RJ (2018). Modeling as a decision support tool for bovine tb control programs in wildlife. Frontiers in Veterinary Science 5, 276.
|
[76] |
Soarimalala V, Randriamanana JP, Onjaniaina G et al. (2019). Les rats dans le monde rural du Centre-est et du Centre-sud de Madagascar: Dommages causés et systèmes de contrôle. Malagasy Nature 13, 125–51.
|
[77] |
Stuart AM, Kong P, Then R, Flor RJ, Sathya K (2020). Tailor-made solutions to tackle rodent pests of rice through community-based management approaches in Cambodia. Crop Protection 135, 104717.
|
[78] |
Stuart AM, Singleton GR, Prescott CV (2015). Population ecology of the Asian house rat (Rattus tanezumi) in complex lowland agroecosystems in the Philippines. Wildlife Research 42, 165–75.
|
[79] |
Sullivan TP, Sullivan DS, Hogue EJ (2001). Reinvasion dynamics of northern pocket gopher (Thomomys talpoides) populations in removal areas. Crop Protection 20, 189–98.
|
[80] |
Sullivan TP, Sullivan DS, Ransome D et al. (2003). Impact of removal-trapping on abundance and diversity attributes in small-mammal communities. Wildlife Society Bulletin 31, 464–74.
|
[81] |
Theuerkauf J, Rouys S, Jourdan H et al. (2011). Efficiency of a new reverse-bait trigger snap trap for invasive rats and a new standardised abundance index. Annales Zoologici Fennici 48, 308–18.
|
[82] |
Whisson DA, Quinn JH, Collins KC (2007). Home range and movements of roof rats (Rattus rattus) in an old-growth riparian forest, California. Journal of Mammalogy 88, 589–94.
|
[83] |
White GC, Burnham KP (1999). Program MARK: Survival estimation from populations of marked animals. Bird Study 46, S120–39.
|
[84] |
Zhang Z, Pech R, Davis S, Shi D, Wan X, Zhong W (2003). Extrinsic and intrinsic factors determine the eruptive dynamics of Brandt's voles Microtus brandti in Inner Mongolia, China. Oikos 100, 299–310.
|
/
〈 | 〉 |